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Int J Syst Evol Microbiol 54 (2004), 1877-1882; DOI  10.1099/ijs.0.63092-0
© 2004 International Union of Microbiological Societies

Bullera cylindrica sp. nov., Bullera hubeiensis sp. nov. and Bullera nakasei sp. nov., ballistoconidium-forming yeast species from plant leaves

Qi-Ming Wang1, Feng-Yan Bai1, Hui-Zhong Lu1, Jian-Hua Jia1 and Masako Takashima2

1 Systematic Mycology and Lichenology Laboratory, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100080, China
2 Japan Collection of Microorganisms, RIKEN (The Institute of Physical and Chemical Research), Wako, Saitama, 351-0198, Japan

Correspondence
Feng-Yan Bai
baify{at}sun.im.ac.cn


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Among yeasts isolated from plant leaves collected in different regions of China that form whitish or yellowish colonies and symmetrical ballistoconidia, four strains were shown to represent three novel Bullera species by conventional and molecular taxonomic characterization. The novel species are described as Bullera cylindrica sp. nov. (type strain CB 169T=AS 2.2308T=CBS 9744T), Bullera hubeiensis sp. nov. (type strain HX 19.3T=AS 2.2466T=CBS 9747T) and Bullera nakasei sp. nov. (type strain HX 15.5T=AS 2.2435T=CBS 9746T). These three species, and another eight previously described Bullera species represented by Bullera mrakii, formed a strongly supported distinct clade among the hymenomycetous yeasts in each of the phylogenetic trees drawn from the 26S rDNA D1/D2 domain and the internal transcribed spacer region sequences.

Abbreviations: ITS, internal transcribed spacer

Published online ahead of print on 5 March 2004 as DOI 10.1099/ijs.0.63092-0.

The GenBank/EMBL/DDBJ accession numbers for the ITS region and 26S rDNA D1/D2 domain sequences determined in this study are AY487563–AY487570, AB118870 and AB118871.

A phylogenetic tree showing relationships between the three novel Bullera species and related taxa is available as supplementary material in IJSEM Online.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
In the Cryptococcus luteolus lineage of hymenomycetous yeasts defined on the basis of 18S rDNA sequence analysis (Takashima & Nakase, 1999Go), two species isolated from plants collected in New Zealand, Bullera mrakii and Bullera huiaensis (Hamamoto & Nakase, 1996Go), form a distinct clade. Three additional Bullera species isolated from the Ogasawara Islands, Japan, were added to the clade by Sugita et al. (1999)Go. The number of species in the clade was increased to eight by Bai et al. (2001)Go, who identified three novel Bullera species among strains originally assigned to Bullera variabilis and assigned these species to the B. mrakii clade by 18S rRNA gene and internal transcribed spacer (ITS) region sequence analyses. None of the species in this clade were studied by Fell et al. (2000)Go or Scorzetti et al. (2002)Go.

Recently, three novel Bullera species belonging to the B. mrakii clade were found among ballistoconidium-forming yeast strains isolated from plant leaves collected in China. The present study supports the distinct nature of the B. mrakii clade in basidiomycetous yeasts of the Tremellales group.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Yeast strains and phenotypic characterization.
Four strains were examined in the present study. Strain CB 169T was isolated from a wilting leaf of Brachybotrys paridiformis collected on Changbai Mountain, Jilin Province, in October 1998. Strains HX 15.5T and HX 19.3T were isolated from wilting leaves of Litsea sp. and Tilia sp., respectively, collected in Hubei Province in October 2002. Strain ST 19.14 was isolated from a wilting leaf of Pinus armandii collected in Shan'xi Province in October 2002. Yeast strain isolation was performed using the improved ballistoconidia-fall method (Nakase & Takashima, 1993Go).

Morphological, physiological and biochemical characteristics were examined according to standard methods (Yarrow, 1998Go). Assimilation of nitrogen compounds was investigated on solid media with starved inocula (Nakase & Suzuki, 1986Go). Extraction, purification and identification of ubiquinones were carried out according to Yamada & Kondo (1973)Go.

Sequence analysis.
Nuclear DNA was extracted by the method of Makimura et al. (1994)Go. Sequencing of the ITS (including 5.8S rDNA) and 26S rDNA D1/D2 domain and molecular phylogenetic analysis were performed using methods described previously (Bai et al., 2002aGo).


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Morphology and chemotaxonomy
The four strains studied formed whitish colonies and reproduced asexually by polar or multilateral budding and production of rotationally symmetrical ballistoconidia. Stalked conidia were not produced. The major ubiquinone was Q-10. Sexual cycles were not observed in single strains or mixed cultures. According to the current taxonomy of basidiomycetous yeasts (Boekhout, 1998Go; Boekhout & Nakase, 1998Go), these strains were assigned to genus Bullera.

rDNA sequence analysis
Three taxa were recognized among the four strains studied from the rDNA sequence comparisons. Strains HX 15.5T and ST 19.14 had identical D1/D2 and ITS sequences. CB 169T and HX 19.3T differed markedly from each other and from the other two strains in the same rDNA regions.

In the phylogenetic tree drawn from the D1/D2 sequence alignment, the three taxa formed three distinct branches in the B. mrakii clade (Fig. 1Go). This clade was strongly supported (100 %) by bootstrap analysis. In the tree drawn from ITS sequences, the B. mrakii clade was also resolved with 100 % bootstrap support (phylogenetic tree available as supplementary material in IJSEM Online). Strains CB 169T and HX 15.5T clustered in a subclade with B. mrakii and four other described species in both the D1/D2 and ITS trees. Strain CB 169T differed from the other taxa in the subclade by 7–19 nt (1·4–3·1 %) and 29–40 nt (>7 %) in the D1/D2 and ITS regions, respectively. Strain HX 15.5T differed from the other taxa in the same subclade by 13–19 nt (2·1–3·1 %) and 39–58 nt (>10 %) in the D1/D2 and ITS regions, respectively.



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  		Fig. 1. Phylogenetic tree drawn from neighbour-joining analysis of the 26S rDNA D1/D2 domain sequences, depicting the relationships of the three novel Bullera species with closely related taxa. Bootstrap percentages over 50 % from 1000 bootstrap replicates are shown. Reference sequences were retrieved from GenBank/DDBJ; accession numbers are indicated.

 
Strain HX 19.3T occupied a basal position in the B. mrakii clade in the D1/D2 tree (Fig. 1Go). It differed from the other taxa in this clade by 19–24 nt (3·0–4·0 %). In the ITS tree, the position of HX 19.3T was slightly different. This strain formed a less well supported subclade together with Bullera komagatae, Bullera schimicola and Bullera pseudoschimicola in the ITS tree (available as supplementary material in IJSEM Online) and differed from these species by more than 100 nt in the ITS region.

These data indicated that strains CB 169T, HX 15.5T and HX 19.3T represent three novel Bullera species, for which the names Bullera cylindrica sp. nov., Bullera nakasei sp. nov. and Bullera hubeiensis sp. nov. are proposed.

Characteristics of the B. mrakii clade
The B. mrakii clade recognized in the present study belongs to the Tremellales in the Hymenomycetes (Fell et al., 2000Go; Scorzetti et al., 2002Go). This clade is closely related to taxa in the Luteolus clade of the Tremellales (Scorzetti et al., 2002Go). Interestingly, the B. mrakii clade is composed exclusively of species belonging to the single genus Bullera, although these species are only distantly related to the type species Bullera alba (anamorph of Bulleromyces albus), as showed in Fig. 1Go. This could imply that species in the B. mrakii clade should be moved to a different genus. The precedent is that the genus Dioszegia was reinstated and redefined by rDNA sequence analysis to accommodate both ballistoconidium-forming and other yeast species in a sister clade of the B. mrakii clade (Takashima et al., 2001Go). In addition to the signature sequences in the 18S rDNA, Dioszegia species form orange-coloured colonies (Bai et al., 2002bGo; Takashima et al., 2001Go; Wang et al., 2003Go). Though a sequence signature (AAGCTC) was found near the 3' end of the ITS2 regions of all the species in the B. mrakii clade (data not shown), no particular morphological or physiological characteristics could be found to discriminate species in this clade from other Bullera species. Therefore, it is thought to be premature to propose a new genus for this clade based only on rDNA sequence data at present.

Physiological differences between species in the B. mrakii clade are shown in Table 1Go. B. cylindrica sp. nov. can be distinguished from closely related species by its ability to assimilate nitrate and to grow in vitamin-free medium. B. hubeiensis sp. nov. is distinct in its inability to assimilate D-arabinose, D-ribose, L-rhamnose, salicin and succinate. B. nakasei sp. nov. can be differentiated by the combination of assimilation reactions of L-sorbose, ribitol, nitrite and ethylamine and the formation of starch-like substances.


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  		Table 1. Salient physiological characteristics of species in the Bullera mrakii clade

Species: 1, B. cylindrica sp. nov; 2, B. hubeiensis sp. nov.; 3, B. nakasei sp. nov.; 4, B. boninensis; 5, B. huiaensis; 6, B. komagatae; 7, B. mrakii; 8, B. schimicola; 9, B. pseudohuiaensis; 10, B. pseudoschimicola; 11, B. waltii. +, Positive; –, negative; D, delayed; V, variable; W, weak; DW, delayed and weak.

 
Morphologically, B. cylindrica sp. nov. and B. nakasei sp. nov. are also distinguishable from other species in the B. mrakii clade. The former forms characteristic cylindrical vegetative cells and the latter forms relatively large, somewhat apiculate vegetative cells.

Latin diagnosis of Bullera cylindrica Bai, Wang et Takashima sp. nov.
In YM (Difco) liquido post dies 5 ad 20 °C, cellulae vegetativae ovoideae, ellipsoideae aut cylindratae, 2·5–4·5x5·5–7·5 µm, singulae aut binae. Annulus et sedimentum formantur. In agaro YM post unum mensem ad 20 °C, cultura flavae-cremea, glabra vel rugosa, non-nitida, butyracea, margine glabra. Pseudomycelium formantur. Ballistoconidia napiformia vel subglobosa, 3·5–5·5x3·0–5·0 µm. Fermentatio nulla. Glucosum, galactosum, L-sorbosum (lente et exigue), saccharosum, maltosum, cellobiosum, trehalosum, melibiosum, raffinosum, melezitosum, amylum solubile, D-xylosum, L-arabinosum, D-arabinosum, D-ribosum, L-rhamnosum, D-glucosaminum, D-mannitolum (lente et exigue), galactitolum (lente et exigue), glucitolum, methyl {alpha}-D-glucosidum, salicinum, acidum succinicum et inositolum assimilantur, at non lactosum, inulinum, methanolum, ethanolum, glycerolum, erythritolum, ribitolum, acidum DL-lacticum, acidum citricum nec hexadecanum. Ammonium sulfatum, kalium nitricum, natrum nitrosum, L-lysinum, ethylaminum et cadaverinum assimilantur. Ad crescentiam vitaminum non necessarium est. Maxima temperatura crescentiae: 27 °C. Materia amyloidea iodophila formantur. Urea finditur. Diazonium caeruleum B positivum. Ubiquinonum majus: Q-10. Typus: CB 169T (=AS 2.2308T=CBS 9744T), isolatus ex folio Brachybotrys paridiformis Maxim.

Description of Bullera cylindrica Bai, Wang & Takashima sp. nov.
Bullera cylindrica (cy.lin'dri.ca. L. nom. fem. adj. cylindrica referring to the cylindrical shaped vegetative cells of the species).

In YM broth, after 5 days at 20 °C, cells are ovoid, ellipsoidal or cylindrical, 2·5–4·5x5·5–7·5 µm, and occur singly or in pairs (Fig. 2aGo). Budding is polar. A sediment and a ring are formed. On YM agar, after 1 month at 20 °C, the streak culture is yellowish cream, butyrous, dull, smooth or somewhat wrinkled. The margin is entire. In Dalmau plate culture on cornmeal agar, pseudohyphae are formed. Ballistoconidia are produced on cornmeal agar and are napiform or subglobose, 3·5–5·5x3·0–5·0 µm (Fig. 2bGo). Fermentation of glucose is negative. Glucose, galactose, L-sorbose (delayed and weak), sucrose, maltose, cellobiose, trehalose, melibiose, raffinose, melezitose, soluble starch, D-xylose, L-arabinose, D-arabinose, D-ribose, L-rhamnose, D-glucosamine, galactitol (delayed and weak), D-mannitol (delayed and weak), D-glucitol, methyl {alpha}-D-glucoside, salicin, succinic acid and inositol are assimilated. Lactose, inulin, methanol, ethanol, glycerol, erythritol, ribitol, DL-lactic acid, citric acid and hexadecane are not assimilated. Ammonium sulfate, potassium nitrate (delayed), sodium nitrite, L-lysine, ethylamine hydrochloride and cadaverine dihydrochloride are assimilated. Maximum growth temperature is 27 °C. Growth in vitamin-free medium is positive. Starch-like substances are produced. Growth on 50 % (w/w) glucose/yeast extract agar is negative. Urease activity is positive. Diazonium blue B reaction is positive. The major ubiquinone is Q-10. The type strain, CB 169T (=AS 2.2308T=CBS 9744T), was isolated from a wilting leaf of Brachybotrys paridiformis Maxim. collected in Changbai Mountain, northeast China in October, 1998.



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  		Fig. 2. Bullera cylindrica sp. nov. CB 169T vegetative cells grown in YM broth for 5 days at 20 °C (a) and ballistoconidia produced on cornmeal agar after 5 days at 20 °C (b). Bars, 10 µm.

 
Latin diagnosis of Bullera hubeiensis Bai, Wang et Takashima sp. nov.
In YM (Difco) liquido post dies 5 ad 20 °C, cellulae vegetativae ovoideae aut ellipsoideae, 2·5–4·5x5·0–7·5 µm, singulae, binae aut adhaerentes. Annulus et sedimentum formantur. In agaro YM post unum mensem ad 20 °C, cultura cremea aut gilvo-flavae, non-nitida, glabra vel rugosa, butyracea, margine glabra aut erosa. Pseudomycelium formantur. Ballistoconidia napiformia vel subglobosa, 3·7–5·0x4·9–6·2 µm. Fermentatio nulla. Glucosum, galactosum, saccharosum, maltosum, cellobiosum, trehalosum, melibiosum, raffinosum, melezitosum, D-xylosum, L-arabinosum, galactitolum (exigue), D-mannitolum (exigue), glucitolum, methyl {alpha}-D-glucosidum (exigue) et inositolum (exigue) assimilantur, at non L-sorbosum, lactosum, inulinum, amylum solubile, D-arabinosum, D-ribosum, L-rhamnosum, D-glucosaminum, methanolum, ethanolum, glycerolum, erythritolum, ribitolum, salicinum, acidum DL-lacticum, acidum succinicum, acidum citricum nec hexadecanum. Ammonium sulfatum et L-lysinum assimilantur, at non kalium nitricum, natrum nitrosum, ethylaminum nec cadaverinum. Vitaminae externae ad crescentiam necessaria sunt. Maxima temperatura crescentiae: 22 °C. Materia amyloidea iodophila non formantur. Urea finditur. Diazonium caeruleum B positivum. Ubiquinonum majus: Q-10. Typus: HX 19.3T (=AS 2.2466T=CBS 9747T), isolatus ex folio Tilia sp.

Description of Bullera hubeiensis Bai, Wang & Takashima sp. nov.
Bullera hubeiensis (hu.be.i.en'sis. L. nom. masc. adj. hubeiensis referring to Hubei Province, China, the geographical origin of the species).

In YM broth, after 5 days at 20 °C, cells are ellipsoidal or ovoid, 2·5–4·5x5·0–7·5 µm, and occur singly, in pairs or in clusters (Fig. 3aGo). Budding is multilateral. A ring and a sediment are formed. On YM agar, after 1 month at 20 °C, the streak culture is cream to light yellow, butyrous, dull, smooth and somewhat wrinkled. The margin is entire or eroded. In Dalmau plate culture on cornmeal agar, pseudohyphae are formed. Ballistoconidia are produced on cornmeal agar and are napiform or subglobose, 3·7–5·0x4·9–6·2 µm (Fig. 3bGo). Fermentation of glucose is negative. Glucose, galactose, sucrose, maltose, cellobiose, trehalose, melibiose, raffinose, melezitose, D-xylose, L-arabinose, galactitol (weak), D-mannitol (weak), D-glucitol, methyl {alpha}-D-glucoside (weak) and inositol (weak) are assimilated. L-Sorbose, lactose, inulin, soluble starch, D-arabinose, D-ribose, L-rhamnose, D-glucosamine, methanol, ethanol, glycerol, erythritol, ribitol, salicin, DL-lactic acid, succinic acid, citric acid and hexadecane are not assimilated. Ammonium sulfate and L-lysine are assimilated. Potassium nitrate, sodium nitrite, ethylamine hydrochloride and cadaverine dihydrochloride are not assimilated. Maximum growth temperature is 22 °C. Growth in vitamin-free medium is negative. Starch-like substances are not produced. Growth on 50 % (w/w) glucose/yeast extract agar is negative. Urease activity is positive. Diazonium blue B reaction is positive. The major ubiquinone is Q-10. The type strain, HX 19.3T (=AS 2.2466T=CBS 9747T), was isolated from a wilting leaf of Tilia sp. collected in Xingshan County, Hubei Province, China in October, 2002.



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  		Fig. 3. Bullera hubeiensis sp. nov. HX 19.3T vegetative cells grown in YM broth for 5 days at 20 °C (a) and ballistoconidia produced on cornmeal agar after 5 days at 20 °C (b). Bars, 10 µm.

 
Latin diagnosis of Bullera nakasei Bai, Wang et Takashima sp. nov.
In YM (Difco) liquido post dies 5 ad 20 °C, cellulae vegetativae ovoideae, ellipsoideae aut apiculatae, 2·0–6·0x6·2–14·5 µm, singulae aut binae. Annulus et sedimentum formantur. In agaro YM post unum mensem ad 20 °C, cultura cremea aut gilvo-flavae, nitida aut non-nitida, glabra vel rugosa, butyracea, margine glabra aut erosa. Mycelium formantur. Ballistoconidia napiformia vel subglobosa, 3·2–7·4x4·5–8·7 µm. Fermentatio nulla. Glucosum, galactosum, L-sorbosum, saccharosum, maltosum, cellobiosum, trehalosum, melibiosum, raffinosum, melezitosum, amylum solubile (exigue), D-xylosum, L-arabinosum, D-arabinosum, D-ribosum, L-rhamnosum, erythritolum (lente et exigue), D-mannitolum (lente et exigue), glucitolum, methyl {alpha}-D-glucosidum, salicinum, acidum succinicum et inositolum assimilantur, at non lactosum, inulinum, D-glucosaminum, methanolum, ethanolum, glycerolum, ribitolum, galactitolum, acidum DL-lacticum, acidum citricum nec hexadecanum. Ammonium sulfatum, L-lysinum et ethylaminum assimilantur, at non kalium nitricum, natrum nitrosum nec cadaverinum. Vitaminae externae ad crescentiam necessaria sunt. Maxima temperatura crescentiae: 27 °C. Materia amyloidea iodophila non formantur. Urea finditur. Diazonium caeruleum B positivum. Ubiquinonum majus: Q-10. Typus: HX 15.5T (=AS 2.2435T=CBS 9746T), isolatus ex folio Litsea sp.

Description of Bullera nakasei Bai, Wang & Takashima sp. nov.
Bullera nakasei (na.ka.se.i. L. gen. masc. n. nakasei in honour of Dr Takashi Nakase, Japan, for his outstanding contributions to the progress of systematics of ballistoconidium-forming yeasts).

In YM broth, after 5 days at 20 °C, cells are ovoid, ellipsoidal or apiculate, 2·0–6·0x6·2–14·5 µm, and occur singly or in pairs (Fig. 4aGo). Budding is multilateral. Sediment and a ring are formed. On YM agar, after 1 month at 20 °C, the streak culture is cream to light yellow, butyrous, semi-shiny to dull, smooth and somewhat wrinkled. The margin is entire or eroded. In Dalmau plate culture on cornmeal agar, true hyphae are formed. Ballistoconidia are produced on cornmeal agar and are napiform, subglobose or somewhat trigonal, 3·2–7·4x4·5–8·7 µm (Fig. 4bGo). Fermentation of glucose is negative. Glucose, galactose, L-sorbose, sucrose, maltose, cellobiose, trehalose, melibiose, raffinose, melezitose, soluble starch (weak), D-xylose, L-arabinose, D-arabinose, D-ribose, L-rhamnose, erythritol (delayed and weak), D-mannitol (delayed and weak), D-glucitol, methyl {alpha}-D-glucoside, salicin, succinic acid and inositol are assimilated. Lactose, inulin, D-glucosamine, methanol, ethanol, glycerol, ribitol, galactitol, DL-lactic acid, citric acid and hexadecane are not assimilated. Ammonium sulfate, L-lysine and ethylamine hydrochloride are assimilated. Potassium nitrate, sodium nitrite and cadaverine dihydrochloride are not assimilated. Maximum growth temperature is 27 °C. Growth in vitamin-free medium is negative. Starch-like substances are not produced. Growth on 50 % (w/w) glucose/yeast extract agar is negative. Urease activity is positive. Diazonium blue B reaction is positive. The major ubiquinone is Q-10. The type strain, HX 15.5T (=AS 2.2435T=CBS 9746T), was isolated from a wilting leaf of Litsea sp. collected in Xingshan County, Hubei Province, China in October, 2002.



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  		Fig. 4. Bullera nakasei sp. nov. HX 15.5T vegetative cells grown in YM broth for 5 days at 20 °C (a) and ballistoconidia produced on cornmeal agar after 5 days at 20 °C (b). Bars, 10 µm.

 


   ACKNOWLEDGEMENTS
 
We thank Professor J.-Y. Zhuang, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China, for identifying the plant samples. This study was supported by grants no. 30170002 from the National Natural Science Foundation of China (NSFC) and no. 2001AA227131 of the ‘863 program’ from the Ministry of Science and Technology, China.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Bai, F.-Y., Takashima, M. & Nakase, T. (2001). Phylogenetic analysis of strains originally assigned to Bullera variabilis: descriptions of Bullera pseudohuiaensis sp. nov., Bullera komagatae sp. nov. and Bullera pseudoschimicola sp. nov. Int J Syst Evol Microbiol 51, 2177–2187.[Abstract]

Bai, F.-Y., Zhao, J.-H., Takashima, M., Jia, J.-H., Boekhout, T. & Nakase, T. (2002a). Reclassification of the Sporobolomyces roseus and Sporidiobolus pararoseus complexes, with the description of Sporobolomyces phaffii sp. nov. Int J Syst Evol Microbiol 52, 2309–2314.[Abstract]

Bai, F.-Y., Takashima, M., Jia, J.-H. & Nakase, T. (2002b). Dioszegia zsoltii sp. nov., a new ballistoconidium-forming yeast species with two varieties. J Gen Appl Microbiol 48, 17–23.

Boekhout, T. (1998). Diagnostic descriptions of and key to presently accepted heterobasidiomycetous genera. In The Yeasts, a Taxonomic Study, 4th edn, pp. 627–634. Edited by C. P. Kurtzman & J. W. Fell. Amsterdam: Elsevier.

Boekhout, T. & Nakase, T. (1998). Bullera Derxii. In The Yeasts, a Taxonomic Study, 4th edn, pp. 731–741. Edited by C. P. Kurtzman & J. W. Fell. Amsterdam: Elsevier.

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Wang, Q.-M., Bai, F.-Y., Zhao, J.-H. & Jia, J.-H. (2003). Dioszegia changbaiensis sp. nov., a basidiomycetous yeast species isolated from northeast China. J Gen Appl Microbiol 49, 295–299.

Yamada, Y. & Kondo, K. (1973). Coenzyme Q system in the classification of the yeast genera Rhodotorula and Cryptococcus and the yeast-like genera Sporobolomyces and Rhodosporidium. J Gen Appl Microbiol 19, 59–77.

Yarrow, D. (1998). Methods for the isolation, maintenance and identification of yeasts. In The Yeasts, a Taxonomic Study, 4th edn, pp. 77–100. Edited by C. P. Kurtzman & J. W. Fell. Amsterdam: Elsevier.




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INT J SYST EVOL MICROBIOL MICROBIOLOGY J GEN VIROL
J MED MICROBIOL ALL SGM JOURNALS